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Open Access

Research

Is exposure to ionising radiation
associated with childhood cardiac
arrhythmia in the Russian territories
contaminated by the Chernobyl fallout?
A cross-sectional populationbased study
Jean-Rene Jourdain,1 Geraldine Landon,1 Enora Clero,1 Vladimir Doroshchenko,2Aleksandr Silenok,2 Irina Kurnosova,2 Andrei Butsenin,2 Isabelle Denjoy,3Didier Franck,1 Jean-Pierre Heuze,1 Patrick Gourmelon1

To cite: Jourdain J-R,
Landon G, Clero E, et al. Is
exposure to ionising radiation
associated with childhood
cardiac arrhythmia in the
Russian territories contaminatedby the Chernobyl fallout? A
cross-sectional populationbased study. BMJ Open2018;8:e019031. doi:10.1136/
bmjopen-2017-019031►► Prepublication history andadditional material for thispaper are available online. Toview these files, please visit
the journal online (http://​dx.​doi.​
org/​10.​1136/​bmjopen-​2017-​
019031).

J-RJ and GL contributed equally.
Received 8 August 2017
Revised 22 February 2018
Accepted 5 March 2018

1

Division of RadiologicalProtection and Health, Institut
de Radioprotection et de Sûreté
Nucléaire (IRSN), Fontenay-auxRoses, France
2
Department of Cardiology,
Bryansk Diagnostic Center,
Bryansk, Russia
3
Department of Cardiology,
Bichat Hospital (AP-HP), Paris,
FranceCorrespondence to
Dr Jean-Rene Jourdain;​jean-​rene.​jourdain@​irsn.f​ r

Abstract
Objective To investigate childhood cardiac arrhythmia andchronic exposure to caesium-137 (137Cs) resulting from the
Chernobyl accident.
Design Prospective cross-sectional study using exposed/
unexposed design conducted in the Bryansk region fromMay 2009 to May 2013 on children selected on the basisof 137Cs soil deposition: control territories ([137Cs]<37 kBq
per square metre, where children were considered as
unexposed) and contaminated territories ([137Cs]>555 kBq
per square metre, where children were considered as
exposed).
Setting Russian territories affected by the Chernobyl
fallout (Bryansk region).
Participants This cross-sectional study included 18 152
children aged 2–18 years and living in the Bryansk region(Russia).
Main outcome measures All children received three
medical examinations (ECG, echocardiography and 137Cs
whole-body activity measurement) and some of them were
given with a 24-hour Holter monitoring and blood tests.
Results Cardiac arrhythmia was diagnosed in 1172
children living in contaminated territories and 1354
children living in control territories. The crude prevalence
estimated to 13.3% in contaminated territories was
significantly lower than in control territories with 15.2%
over the period 2009–2013 (P<0.001). Considering 137Cs
whole-body burden as exposure, cardiac arrhythmia
was found in 449 contaminated children and 2077
uncontaminated children, corresponding to an estimatedcrude prevalence of 14.5% and 14.2%, respectively, which
does not differ significantly (P=0.74). Also, we investigated
the association between territory, exposure to 137Cs andcardiac arrhythmia: the adjusted OR was not significant(0.90 with 95% CI 0.81 to 1.00; P=0.06) for the territory.
For 137Cs whole-body burden, the ORs close to 1 did notreach statistical significance (P for trend=0.97).
Conclusion This study does not observe an association
between cardiac arrhythmia and 137Cs deposition levelsin the Bryansk region exposed to Chernobyl fallout. The

Strengths and limitations of this study►► This study includes a large number of participants

and a nice participation rate (91%). There is very
little missing data (<1%).
►► Conditions were met to show an effect if it would
exist: the minimal detectable OR was estimated tobe 1.2.
►► Comprehensive information on potential previous
homes of children included in the study was notavailable. In particular, we do not know if they wereborn in a contaminated territory or not.
►► Some factors that may play a role in the occurrenceof a cardiac arrhythmia have not been considered,such as hypertension, genetic factors and consumption of tobacco, alcohol or drugs.
►► ECGs and echocardiography examinations were performed only once on each child.

suspected increase of cardiac arrhythmia in children
exposed to Chernobyl fallout is not confirmed.

Introduction
On 26 April 1986, the worst industrial accident that released worldwide man-madeenvironmental ionising radiation occurredat the Reactor Number 4 of the Chernobyl
nuclear power plant in the former Soviet
Union. The radioactive fallout that spread
mainly over northern Ukraine, southwestern
Russia and Belarus as a result of the tragedy
reached a total of about 13.1018 Becquerel(Bq). It heavily exposed a large populationof about 5 million individuals at the time of
the accident, including around 1.2 million
children and adolescents, to a mixture of

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radionuclides among which iodine-131 and caesium-137(137Cs) are the most significant for the dose received by
the affected people.1 2 Apart from Chernobyl cohorts,
the health effects of acute and protracted exposures toenvironmental radiation as a result of a nuclear event
have been and are being widely studied, mainly in theJapanese survivors of the Hiroshima and Nagasaki bombings, and since March 2011 in the population exposed to
the releases from the Fukushima Dai-chi nuclear power
plant. Depending on the type of radiation exposure,dose rate and study population, short-term and long-term
health risks of nuclear power plant accidents may include
acute radiation syndrome, elevated rate of leukaemia
and solid cancers, cataracts, circulatory diseases andincrease in childhood thyroid cancers.1–10 Besides thesewidely recognised radiation-induced pathologies, someauthors claimed that exposed children may also exhibit
various symptoms including chronic gastrointestinal
pathology, gallbladder inflammation, chronic periodontitis, asthenia, apathy, tonsil hypertrophy, recurrent respiratory infections, endocrine disorders andcardiovascular symptoms, such as unstable blood pressure, sinus arrhythmia, repolarisation and conduction
abnormalities.11–14 However, these observations are stillquestionable as they are not based on significant statisticalevidence and the causal link with an exposure to ionisingradiation has not been demonstrated so far. Because
the related publications have led to a recurrent debate
and in the absence of well-designed studies, the Institut
de Radioprotection et de Sûreté Nucléaire decided in
2005, together with the Russian Bryansk Diagnostic
Center, to launch a research programme named ‘EPICE’(acronym for ‘Evaluation of Pathologies potentially
Induced by CaEsium’) aiming to explore the non-cancer
effects exhibited in children living in Russian territories
contaminated by the Chernobyl fallout versus control
territories. This article presents the design and resultsof the first study that has been carried out in a group of
about 18 000 Russian children to determine whether they
suffer from cardiac arrhythmia and, if so, to confirm or
refute the possible association with a chronic exposure to137
Cs, the major radionuclide to which the local population is still being exposed significantly more than 30 years
after the Chernobyl catastrophe.

areas are defined as those with 137Cs deposition levels >37 kBq
per square metre.15 16 Therefore, we have considered in ourstudy control territories as territories with [137Cs]<1 Ci(Curie) per square kilometre or 37 kBq per square metre(where children were considered as unexposed) and,contaminated territories as territories with [137Cs]>15 Ci
per square kilometre or 555 kBq per square metre(where children were considered as exposed). The flow
chart presented in figure 1 illustrates the inclusion of thesubjects.
With regards to the control territories, the nineraions (a raion is a type of administrative unit of several
post-Soviet states; the Bryansk region named ‘Bryansk
oblast’ is divided into 27 raions) totally unpolluted with137
Cs were selected. Four were excluded due to the presence of polluting chemical plants and substantial differences especially related to diet. To reach the targeted
number of participants, a sixth raion was selected
randomly among 14 raions comprising control territories
and territories with 137Cs soil deposition between 37 and75 kBq per square metre. Children of this sixth raion camefrom unpolluted areas. Therefore, six raions (Zhukovsky,
Kletnjansky, Dubrovsky, Rognedinsky, Zhiryatinsky and
Bryansky) were found to be eligible for inclusion in the
study. As of contaminated territories, the five raions wereselected except one because of substantial population
relocations (Novozybkovsky, Gordeevsky, Zlynkovsky andKrasnogorsky). Among eligible children 1794 did not
accept to be surveyed because of various specific reasons(religious grounds, sport competition, fear of not being
accepted in sport clubs or military institutions, refusal
to undress, recent similar medical examination andongoing medical care). Finally, out of 18 152 children
examined, 455 children were excluded from the analysis
because either they were suffering from a disease otherthan cardiac arrhythmia or from another disease leading
to cardiac arrhythmia. Thus, the study included a total of
17 697 children.
Procedures
Data were collected by a Russian health professional team(interviewers, ultrasound practitioners, nurses, cardiologists and dosimetrists) who were on the field to meetchildren at schools where medical examinations wereconducted. An informed consent was obtained fromchildren or their parents. The participation in this study
consisted first in completing a questionnaire and thenundergoing several medical explorations.

Methods
Study design
This cross-sectional study using exposed/unexposed
design was approved and validated by the Ethics
Committee of the Russia’s National Hematology Centerin Moscow. It was conducted in the region of Bryansk
from May 2009 to May 2013 on children aged 2–18 years.
This study primarily intended to compare populations
living in the least contaminated territories with thoseliving in the most heavily contaminated territories. Children were selected on the basis of 137Cs soil deposition:according to two international entities, contaminatedQuestionnaire
Each study participant was assigned with a personal
number notified in an administrative and medical questionnaire bringing together all necessary information(administrative, demographic and anthropometric data;anamnesis targeted on cardiovascular area; results ofwhole-body 137Cs activity, ECG, echocardiography and,
when performed, a 24-hour Holter monitoring and blood
tests; and conclusions of the cardiologist).

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Open AccessFigure 1

Flow chart of inclusion criteria. 137Cs, 137-caesium.

Creatine kinase (CK)), biochemical (Sodium (Na),Potassium (K), Calcium (Ca), Phosphorus (P), albumin),inflammatory (C-reactive protein (CRP)), renal (urea,
creatinine), thyroid (Thyroid-stimulating hormone(TSH), Free thyroxine (FT4)) and cardiac (troponin T,
Creatine kinase-MB (CK-MB)) profiles were performed.
For blood assays, biologists employed a 9180 electrolyte analyser (Roche Diagnostics), an automated
Enzyme immuno-assay (EIA) and chemistry analyser
ChemWell (Awareness Technology), a biochemical analyser SYNCHRON CX4-CE (Beckman Coulter), a LIANA
luminometer (Immunotech S.A.S.) and the Roche TROP
T sensitive rapid assay.

Medical examination
After assessing their weight and height, all children were subjected to a direct measurementof whole-body 137Cs activity performed with aradiometer-spectrometer RSU-01 ‘Signal-M’. The 137Cs
background activity was systematically assessed andsubtracted from activity measured in children. The detection limit (DL) was evaluated to be around 1200 Bq for a
10 min counting time depending essentially on the background activity. Then, children underwent an ECG. The
recorder was the CardioSoft V.6.5 resting ECG (GE Medical
Systems Information Technologies). ECG was performedat rest for about 10 min and tracings were available forall children in the database. An echocardiography was
also carried out using an ultrasound diagnostic scanner
MyLab 30 CV (ESAOTE) with a phased array probe. For
each echocardiography performed, among collected data
we investigated more closely the following parameters:
left ventricular diameter at end-systole, left ventricular
diameter at end-diastole, left ventricle ejection fraction,left ventricular posterior wall thickness at end-diastole,
left ventricle velocity, interventricular septum thickness
at end-diastole, right ventricular diameter at end-diastole,
mitral inflow velocity, left atrial diameter, aortic diameter,
tricuspid peak velocity, trunk diameter of the pulmonary
artery and pulmonary artery velocity; a later publication is
being prepared to further explore these data. Only ultrasound images of pathological cases have been recorded
into the database. For some randomly selected children,a 24-hour Holter monitoring was recorded with a CardioDay (Getemed Medizin). Blood tests to assess enzymatic(transaminases, Alkaline phosphatase (ALP), Lactate dehydrogenase (LDH), Gamma-glutamyltransferase (GGT),

Statistical analyses
The characteristics of the study population were describedby number (percentages) for categorical variables andby mean (min–max) and median for continuous variable (‘caesium burden’: 137Cs whole-body burden). Ageat diagnosis was categorised into tertiles based on the

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Medical diagnosis of cardiac arrhythmia
The diagnoses of cardiac arrhythmia (including cardiac
conduction and cardiac rhythm disorders)17 have beenregistered according to WHO’s International Classification of Diseases Tenth Revision (2010).18 Pathologies/
syndromes identified in the course of the study belong
to the following categories: atrioventricular and left
bundle-branch block (I44.0; I44.1; I44.2; I44.4; I44.5);
other conduction disorders (I45.0; I45.1; I45.2; I45.4;
I45.5; I45.6; I45.8); paroxysmal tachycardia (I47.1); othercardiac arrhythmias (I49.1; I49.3; I49.4; I49.5; I49.8); andabnormalities of heart beat (R00.0; R00.1).

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distribution among healthy children (<10, 10–13, ≥14years). Body mass index (BMI) was calculated as weight(kg) divided by squared height (m) and was categorised
according to age and sex as recommended by WHO(underweight, normal weight, overweight, obesity).19
As of ionising radiation exposure variables, two wereconsidered: ‘territory’ (control, contaminated); ‘caesium
burden’, which was categorised into quartiles based on
the distribution among healthy children with a positive
whole-body contamination (not detectable; ]DL–35[;[35-50[; [50-70[;≥70 Bq/kg). The associations between
territory or caesium burden and cardiac arrhythmia risk
were analysed using a non-conditional logistic regression.20 In multivariate analysis, all ORs with 95% CIs were
adjusted for variables having a P value<0.25 on univariate analysis. Tests for interaction were performed toassess whether territory or caesium burden association
with the presence of cardiac arrhythmia risk were modified by parameters such as BMI, drug intake with cardiac
arrhythmia as side effects, caesium burden or territory.
A generalised linear model was used to determine thecontribution of each variable to the caesium burden.
Sensitivity analysis on children with cardiac arrhythmia
who underwent blood test was conducted using χ2 test.
Other sensitivity analyses were undertaken on children
with cardiac conduction disorders only, children withcardiac rhythm disorders only or all children diagnosed
with also sinus arrhythmia. Statistical tests were two-sided
and P values<0.05 were considered statistically significant.
Tests for trend were performed by considering categorical variables as continuous variables using the Wald χ2
statistic. All data were analysed with the use of SAS software V.9.2 (SAS Institute).

Results
The study included 8816 exposed and 8881 unexposedchildren. Table 1 shows all characteristics of participants.
Males and females were almost equally represented,
and distribution of children by age category was quite
similar. All children underwent three medical examinations (ECG, echocardiography and 137Cs whole-body
activity measurement) and a 24-hour Holter monitoring
was performed in 15.6% and 27.2% of exposed andunexposed children, respectively. It is understood thatfor children who were given both an ECG and a 24-hour
Holter monitoring the final diagnosis has consideredsystematically the results of the Holter as a more sensitive examination compared with the ECG. Thereby,

cardiac arrhythmia was diagnosed in 1172 exposedand 1354 unexposed children. The crude prevalence
estimated to be 13.3% in contaminated territories
was significantly lower than in control territories with
15.2% over the period 2009–2013 (P<0.001). The prevalence ratio was 0.87 (95% CI 0.84 to 0.90). Considering
caesium burden as exposure (data not shown), cardiac
arrhythmia was found in 449 contaminated children
and 2077 uncontaminated children, corresponding toan estimated crude prevalence of 14.5% and 14.2%,
respectively, which does not differ significantly (P=0.74)
and resulting in a prevalence ratio of 1.02 (95% CI 0.97
to 1.07).
The distribution of caesium burden was describedby a log-normal shape; 21.4% of children living incontaminated territories had a detectable 137Cs wholebody contamination compared with 13.6% of children
living in control territories (table 1). The distributionof children living in contaminated territories rose withincreasing 137Cs whole-body contamination in contrast
with children living in control territories for whom
the trend was reversed. Indeed, 4.5% and 4.8% of
those children had a 137Cs whole-body contamination<35 Bq/kg, while with 137Cs whole-body contamination
exceeding 70 Bq/kg the gap was widening (7.1% and2.1%, respectively). The calculation of the committed
effective dose in the 3105 children with a detectablecaesium burden showed that only 24 patients were
>1 mSv (with a maximum dose of 5.77 mSv per year).
As of their lifestyle, characteristics were similar
in both exposed and unexposed children: nearly
two-thirds of children lived in urban area and dietary
habits seemed to be similar except for consumptionof forest products (mushrooms, berries, meat), which
decreased in exposed children (62.2%) comparedwith unexposed children (80.7%). In both territories,
the distribution of children according to BMI categories was balanced. The number of children with a highBMI (overweight and obesity combined) represented
23.5% and 23.9% in contaminated and control areas,
respectively. When the participants were questioned
about drug intake, it happens that a limited numberof children took drugs, 1.2% and 2.9% in the contaminated and control territories, respectively. Amongthe identified drugs, more than three-quarters werevasoconstrictors, antibiotics, antihistaminics andbronchodilators.
In univariate analysis, the risk of cardiac arrhythmia
was significantly decreased with sex, drug intake,
BMI and territory variables (table 2). However, children >14 years had a 2.3-fold increase of cardiac
arrhythmia risk compared with younger children(<10 years). For caesium burden, children withcontamination <35 Bq/kg presented a significant higher
risk of cardiac arrhythmia than children with no detectable contamination (OR 1.37; 95% CI 1.15 to 1.65).
The adjusted OR was no longer significant (0.90 with
95% CI 0.81 to 1.00; P=0.06) for the territory. Similarly,

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Patient involvement
No patients were involved in setting the research question or the outcome measures, nor they were involved
in developing plans for design or implementation of thestudy. No patients were asked to advise on interpretation
or writing up of results. The authors plan to disseminate
the results of the research to study participants throughpublic meetings as soon as the article is published.

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Open Access
Table 1 Description of the study population
Contaminated territories(exposed population)

Control territories(unexposed population)

Characteristics

n=8816n=8881(%)*

Sex Male4436(50.3)

4534(51.1) Female

4380(49.7)

4347(48.9)

 <10

3412

(38.7)

3057(34.4) 10–132598(29.5)

3109(35.0)

 ≥14

2806

(31.8)

2715(30.6)

8816

(100)

8881

(100)

1377

(1536)

2418(27.2)(%)*

Age (years)

Type of medical examination ECG Echocardiography Caesium-137 whole-body activity Holter†
Health condition Healthy

7644(86.7)

7527(84.8) With cardiac arrhythmia (including
cardiac conduction disorders)1172(13.3)

1354(15.2)

Drug intake possibly responsible for cardiac arrhythmia
 No

3933

(44.6)

8335(93.9)

 Yes

108

(1.2)

257

(2.9)

 Unknown

4775(54.2)

289(3.3) Underweight

179

(2.0)

204

(2.3)

 Normal weight6565(74.5)

6550(73.8) Overweight1219(13.8)

1218(13.7) Obesity

853

(9.7)

909

(10.2) Rural area

2833

(32.1)

3165(35.6) Urban area

5983

(67.9)

5716(64.4) Not detectable

6925(78.6)

7667(86.3) ]DL–35[

394

(4.5)

425

(4.8)

 [35–50[

454

(5.1)

349

(3.9)

 [50–70[

413

(4.7)

250

(2.8)

 70 and more

630

(7.1)

190

(2.1)

 Mean‡(min–max)  73.8 (14.3–2137.5)  47.3 (13.2–143.1) Median‡  53.8  41.8

Body mass index (WHO classification)

Place of residence

Caesium burden (Bq/kg)

Dietary habits Shop (clean food)8128(92.2)

7676 Personal farm (milk, meat, vegetables) Forest (mushrooms, berries, meat) Local reservoirs, rivers (fish, crayfish)(86.4)

6448(73.1)

6722(75.7)

5486
3862(62.2)(43.8)

7171
4237(80.7)(47.7)*The percentages may not sum to 100 because of rounding.
†Data were missing for 37 children.
‡Only among children with detectable caesium burden.

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Table 2 Univariate analysis of associated factors related to
cardiac arrhythmia
Associated factors

OR(95% CI)Sex  Male1–  Female

0.66(0.61 to 0.72)

 <10

1

–

  10–13

0.97(0.87 to 1.09)

 ≥14

2.27

(2.06 to 2.51)

P values<0.01

Age (years)<0.01*

Drug intake possibly responsible for cardiac arrhythmia
  No

1

–

  Yes

0.79(0.58 to 1.09)

0.16  Unknown

0.89(0.81 to 0.98)

0.02

Body mass index (WHO classification)  Underweight1– Normal weight

0.88(0.67 to 1.15)  Overweight

0.71(0.53 to 0.95)  Obesity

0.62(0.45 to 0.84)  Control1–  Contaminated

0.85(0.78 to 0.93)

1–<0.01*

Territory<0.01

Caesium burden (Bq/kg) Not detectable  ]DL–35[

1.37(1.15 to 1.65)  [35–50[

0.98(0.80 to 1.20)  [50–70[ 70 and more

0.89
0.84

(0.70 to 1.12)(0.68 to 1.04)

0.17*

The ORs indicated in bold are statistically significant.
*P values for trend.

Table 3 Multivariate logistic regression model for
associated factors in relation to cardiac arrhythmia
Associated factors

OR*(95% CI)

Territory  Control1–  Contaminated

0.90(0.81 to 1.00)

1–

P values

0.06

Caesium burden (Bq/kg) Not detectable  ]DL–35[

1.07(0.89 to 1.29)  [35–50[

1.00(0.81 to 1.23)  [50–70[ 70 and more

1.04
0.96

(0.82 to 1.31)(0.77 to 1.20)

for caesium burden, the ORs close to 1 did not reachstatistical significance (P values for trend=0.97) (table 3).
Thus, there was no evidence of any association between
the presence of cardiac arrhythmia and territory or
caesium burden.
When we paid attention to the caesium burden, theranking in the explanation of the variance of this variable was first territory, age (particularly <10 years), 137Cs
whole-body activity measurement performed during
autumn season and consumption of forest products, byorder of importance (results not shown).
Furthermore, associations between the presence of
cardiac arrhythmia and territory or caesium burden
were not significantly different according to BMI, drug
intake and territory or caesium burden (results notshown).
Finally, we investigated the risk of all diagnosed caseswith sinus arrhythmia cases (considered as pathologicalin Russia), cardiac conduction disorders cases only andcardiac rhythm disorders only (table A in online supplementary appendix). All results were similar to those of
cardiac arrhythmia cases (table 3) except for the relationship between cardiac conduction disorders andterritory for which the OR was statistically significant(0.82; 95% CI 0.69 to 0.99; P=0.04), thereby suggestingthat living in a contaminated territory would notincrease the risk to develop a cardiac arrhythmia.
Another sensitivity analysis was performed for children
with cardiac arrhythmia who had blood tests (n=1079).
The results are shown in table B in online supplementary
appendix.
Among measured blood parameters were included
calcium, potassium, and TSH and FT4 for thyroid function, which are the major biological parameters whose
variations are often observed in a context of a cardiac
arrhythmia.21 22 The proportion of children with hypocalcaemia was significantly higher in control territories
compared with contaminated territories (P=0.001) andthe inverse was observed for children with hyperkalaemia (P=0.004). However, when considering caesium
burden as exposure, no significant differences were
evidenced (P=0.18 for children with hyperkalaemia
and P=0.98 for children with hypocalcaemia) (data notshown). With respect to other biological parametersinvestigated, the sensitivity analysis did not evidence
differences between children living in control territories compared with contaminated territories. Similar
observations were made when considering caesium
burden as exposure (data not shown).

For caesium burden, adjustment for sex, age, drug intake, bodymass index and territory.
*For territory, adjustment for sex, age, drug intake, body massindex and caesium burden.

Discussion
Health consequences of the Chernobyl accident in childreninternally exposed to ionising radiation
The ways that usually characterise human radiation exposure are total or partial body irradiation, external contamination (radioactive particle skin deposit) and internal
contamination (inhalation, ingestion, wound). The latter

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Open Accessroute that implies incorporation inside the body of radioactive material, which is inhaled and/or ingested, is ofparticular importance when assessing the health consequences for exposed children. Thus, while the scientificcommunity was expecting after the Chernobyl accident anincreased incidence in childhood leukaemia as observedin the Hiroshima and Nagasaki survivors, an increase in
the frequency of thyroid cancer in children was observed
since 1990.23 This observation was lately confirmed in a
number of publications along the decades that followed
the accident.1 2 9 10 The childhood thyroid cancer epidemic
is now widely recognised as a major consequence of theChernobyl accident despite doubts that some experts
expressed about the accuracy of diagnosis and becauseof the short period of latency.1 2 Indeed, according to theUnited Nations Scientific Committee on the Effects ofAtomic Radiation (UNSCEAR) 2008 report, 6848 casesof thyroid cancer were reported in the affected territories
of Belarus, Ukraine and Russia between 1991 and 2005
in children under age 18 years in 1986.2 Actually the riskof developing a thyroid cancer after childhood exposure
is known since years as described in an updated pooled
analysis recently published.24 However at the time of theChernobyl accident, radiation-induced thyroid cancer
was recognised as a potential consequence of an external
irradiation only, delivered mainly in the context ofchildhood cancer therapies. In the Chernobyl situation,
children were exposed mostly because of the ingestion offood and milk contaminated with iodine-131, short-lived
radioactive iodines and tellurium. The radioactive iodines
were accumulated into the thyroid, which was often deficient in stable iodine, leading thus to the development of
thyroid cancer in children, especially in those who were
under age 4 years at the time of the accident.
Rationale of this study
To date, thyroid cancer is the only disease undoubtedly
attributable to ionising radiation in exposed Chernobyl
children. However, arguing that children have been
and are still exposed to 137Cs because of the consumption of foodstuffs such as mushrooms and berries locally
produced and contaminated as a result of a transfer ofradionuclides from the soil, some authors attribute toradiation exposure a number of other illnesses exhibited in children living in contaminated territories, suchas various infections, gastric symptoms or cardiovasculardiseases, among cardiac arrhythmias that are frequently
mentioned.14 These authors state that such diseases
would be caused by a chronic incorporation and heterogeneous accumulation of radioactive caesium inside thebody, particularly into the myocardium.11–14 However,there is no indication of an accumulation into the
myocardium in a publication presenting an update of the
biokinetic models for radiocaesium and its progeny as theseradionuclides are known to be distributed mainly in theskeletal muscles.25 Because it was not possible to verify thescientific data put forward by these authors, we decided
to launch the EPICE programme, recognising that it
Jourdain J-R, et al. BMJ Open 2018;8:e019031. doi:10.1136/bmjopen-2017-019031

was not possible for us to address questions that several
non-governmental organisations raised about cardiac
arrhythmias exhibited in exposed children resulting froma chronic incorporation of 137Cs.
To solve the question about a homogenous versus
heterogeneous distribution of caesium into the body,
we performed previously to this study some direct
measurements of 137Cs activity in a group of 49 Russianchildren living in the Bryansk contaminated territories
and suffering from cardiac arrhythmia, gastric symptoms
and lens opacities. This work did not evidence an accumulation of 137Cs in the heart region compared with the neckregion (including the thyroid), the abdominal regionand skeletal muscles. Therefore, our results supported
the hypothesis that 137Cs was homogeneously distributed
inside the body of enrolled children (data not shown).
Study design
Cross-sectional studies do not permit the reconstruction of a time sequence between exposure and observed
disease. The objective of the present study was to compare
the prevalence of a disease between two geographical areas. Indeed, it would have been of added value
to consider time trends in the frequency of arrhythmia
among children after the Chernobyl accident. However,a cross-sectional design is not suitable for spatiotemporalapproaches.
One of the other classical potential biases of this type ofstudy is the lack of control of population migration thatis the capacity to know whether people in each area have
moved since birth. In our study, comprehensive information on potential previous homes of children was notavailable. In particular, we do not know if they were bornin a contaminated territory or not. However, it should
be noted that these populations with limited financial
resources were likely not geographically mobile, notably
because of financial compensations which represented astrong argument that was very carefully considered by thefamilies when deciding on to move or not to move to an
unexposed area.
In our protocol, the control group has been defined
as children living in territories with [137Cs]<37 kBq per
square metre in the Bryansk oblast. We decided not toconsider territories far away from the contamination to
avoid too large differences in terms of socioeconomic
living conditions, which are quite specific to the oblast of
Bryansk compared with other Russian regions.
Comparison with other studies
Two large studies addressing the prevalence of cardiac
conduction disturbances in children have been publishedin the early 21st century. A first survey performed by questionnaire, electrocardiography, phonocardiography andphysical examination was conducted in Taipei, Taiwan,
between 1999 and 2001 in a population of 432 166 elementary and high school students aged from 6 to 20 years.
In this study, the authors, after excluding students withcongenital heart disease, assessed a prevalence of 0.75%.26
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Open Access
A second analysis of disturbances of cardiac rhythm byusing ECG performed as part of a cardiac screening test
was carried out in Chiba City, Japan, between 1996 and2001 in a population of 152 322 children. In this study, theprevalence of disturbances of cardiac rhythm was 1.25%
in elementary school students aged from 5 to 6 years and2.32% in junior high school students aged from 12 to 13
years.27 To our understanding, the two studies mentioned
above were performed in children not exposed to artificial sources of ionising radiation in a context of alarge-scale screening.
Another study explored arrhythmia in infants in the UK(Northern Region of England).28 Nevertheless, this paper
was dealing with incidence and so that conclusions of thisstudy cannot be directly compared with our results since
the present study considered the prevalence of childhood
arrhythmia.
To our knowledge, our study is the largest one having
explored cardiovascular functions among children in acontext of internal radiation contamination. The resultsof our work show a crude prevalence of cardiac arrhythmia
significantly lower in children living in contaminatedversus control territories (13.3% vs 15.2%). Comparedwith the studies performed in Taipei and Chiba, theassessed prevalence seems much higher. However, we
do think that outcomes of our study are not comparable
to those of the two Asian studies. Thus, the numberof children included in our study is much smaller; theexaminations on which we based our diagnosis of cardiac
diseases are more comprehensive (ECG, echocardiography, Holter); and the two studies mentioned above
were performed in Asian children living in very different
socioeconomic conditions compared with our group of
Caucasian children who lived in much more unfavourable conditions.
Very importantly, this study does not observe an association between cardiac arrhythmia and territory or caesium
burden, and even shows a higher number of arrhythmic
patients living in control territories, despite a higher
caesium burden in children enrolled in contaminatedversus control territories. We note that the number of
24-hour Holter monitoring was higher in control territories than in contaminated territories (2418 and 1377,
respectively). Therefore, we cannot exclude that thisdifference in the frequency of Holter may be linked to ahigher number of cardiac arrhythmia in control territories. However, the percentage of children diagnosed witha cardiac arrhythmia on the basis of both positive ECG
and positive Holter is similar in contaminated territories
and control territories (56% and 54%, respectively). In
addition, other factors not related to radiation exposure(eg, lifestyle) may also affect the frequency of arrhythmia
in control territories.
Focusing on the dose assessed in children measured
with a detectable caesium burden, our study shows that
only 24 among 3105 patients (0.8%) have received aradioactive dose above the annual exposure limit of
1 mSv recommended by the International Commission ofRadiological Protection in a normal situation.29 It seems
to argue that the presence of an arrhythmia is related toneither the radioactive dose nor the contamination of
the territory where children lived, which is not directly
proportional to the 137Cs whole burden. Moreover, forthe same ingested amount of 137Cs, some children will
present a high body burden, while for others the radioactive caesium will not be detectable because of theinterindividual variability in the behaviour of caesium inthe body and weight differences from a child to another.
Regarding the effect of the season on the measurement ofwhole-body 137Cs burden, a thorough analysis shows thatamong the 449 children with both cardiac arrhythmia
and whole-body 137Cs activity above the DL, 259 live in thecontaminated territories and 190 in the controlled territories. When looking at the season when the 137Cs measurement was performed, the results show that the majorityof children were measured during the autumn or winter,with a comparable result between contaminated territories (67%) and controlled territories (61%). This result
is, after all, rather not surprising because mushrooms,
berries and game (eg, wild boar meat) are highly eaten
in Russian families mostly along fall and winter. These
forest products are known to be the most heavily contaminated with 137Cs in both contaminated and controlled
territories. Finally we notice that the individuals with adetectable caesium burden and living in contaminatedterritories have been contaminated as a result of a longlasting soil caesium contamination and not because they
were exposed directly to the Chernobyl releases, notably
radioactive iodines, as they were born several years after
the accident.

8

Jourdain J-R, et al. BMJ Open 2018;8:e019031. doi:10.1136/bmjopen-2017-019031

Conclusion
The study presented in this article has been carried out
in the largest group ever observed among children withcardiac arrhythmia in the Russian territories affected by
the Chernobyl fallout. Our results show a higher prevalence of childhood cardiac arrhythmia over the period
2009–2013 in control versus contaminated territories in
the Russian oblast of Bryansk where the study has been
implemented. Also we do not observe an association
between cardiac arrhythmia and 137Cs deposition levelsin the Bryansk region exposed to Chernobyl fallout.
The suspected increase in the frequency of childhood
cardiac arrhythmia that some scientists evoked in children exposed to chronic incorporation of 137Cs is notconfirmed. Therefore, it would not be recommended
to implement a large-scale screening of cardiovasculardiseases in children exposed to radioactive releases rightafter a nuclear accident comparable to the thyroid cancer
screening that started just after the Fukushima accident.30
However, these data may be useful for future comparative study of cardiac arrhythmia in children exposed
to ionising radiation in other contexts, such as cancer
radiation therapies. Also this study offered a unique
opportunity to collect in a very large group of children anDownloaded from http://bmjopen.bmj.com/ on April 5, 2018 - Published by group.bmj.com

Open Access
impressive amount of information related to the normal
limits for the paediatric ECG and echocardiography thatwill certainly help to adjust the diagnostic criteria used so
far by the paediatricians.31 The publication of the resultsof this study will be followed by another article presenting
the results of a large-scale screening of lens opacities ina similar group of children living in the same oblast of
Bryansk. This ongoing study is being achieved and will
hopefully provide some elements of answer to anotherquestion often raised when assessing the health consequences of childhood exposure to ionising radiation after
a nuclear accident.
Acknowledgements The authors thank Dr Dominique Laurier for his advice
relevant to the result interpretation, as well as Dr Cecile Challeton-de Vathaire
and Dr Eric Blanchardon for their help in the assessment of committed dose
received to children enrolled in this study. The authors are also grateful to Dr
Tarita Voldemar and colleagues from the Nikiforov Russian Center of Emergency
and Radiation Medicine, EMERCOM, in St. Petersburg, Russia, for their support inthe calibration of the radiation measurement device used in this study, and to theinterpreters Nathalie Rutschkowsky and Oxana Gouliaeva for having facilitated thecommunication between Russian and French authors.
Contributors PG and JRJ had the idea for the study. JRJ, GL, VD, AS, IK and AB
contributed to the design, the conduct of the study and the recruitment of patients.
VD, AS, IK, and AB contributed to the collection of clinical data. IK contributed to thedesign of the database and the entry of computer data. JRJ, GL and ID contributed
to medical diagnoses consultation. JRJ and GL contributed to literature search anddrafted the report. DF and J-PH contributed to the analysis of dosimetry data. JRJ,
GL and EC contributed to statistical data analysis and interpretation. All authors
critically reviewed the manuscript and approved the final version of the draft. The
research was designed, conducted, analysed and interpreted by the authors entirely
independently of the funding sources.
Funding This study was entirely financed by the IRSN's research budget. Thisbudget is allocated by the ministries to which the IRSN reports, notably the Ministryof Ecology.
Disclaimer The ministries had no role in study design, data collection, data
analysis, data interpretation or writing of the report.

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Competing interests None declared.

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Patient consent Parental/guardian consent obtained.

20.

Ethics approval This study was approved and validated by the Ethics Committeeof the Russia’s National Hematology Center in Moscow. The study was conducted inaccordance with the principles of the Declaration of Helsinki.

21.

Provenance and peer review Not commissioned; externally peer reviewed.

22.

Data sharing statement Under ethical approval, patient-level data cannot bemade available.

23.

Open Access This is an Open Access article distributed in accordance with theCreative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which
permits others to distribute, remix, adapt, build upon this work non-commercially,and license their derivative works on different terms, provided the original work is
properly cited and the use is non-commercial. See: http://​creativecommons.​org/​
licenses/​by-​nc/4​ .​0/
© Article author(s) (or their employer(s) unless otherwise stated in the text of thearticle) 2018. All rights reserved. No commercial use is permitted unless otherwise
expressly granted.

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Downloaded from http://bmjopen.bmj.com/ on April 5, 2018 - Published by group.bmj.com

Is exposure to ionising radiation associatedwith childhood cardiac arrhythmia in the
Russian territories contaminated by the
Chernobyl fallout? A cross-sectional
population-based study
Jean-Rene Jourdain, Geraldine Landon, Enora Clero, Vladimir
Doroshchenko, Aleksandr Silenok, Irina Kurnosova, Andrei Butsenin,
Isabelle Denjoy, Didier Franck, Jean-Pierre Heuze and Patrick
Gourmelon
BMJ Open2018 8:

doi: 10.1136/bmjopen-2017-019031
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http://bmjopen.bmj.com/content/8/3/e019031

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